Phillips, B.T., D.F. Gruber, G. Vasan, V.A. Pieribone, J.S

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CITATION Phillips, B.T., D.F. Gruber, G. Vasan, V.A. Pieribone, J.S. Sparks, and C.N. Roman. 2016. First evidence of bioluminescence on a “black smoker” hydrothermal chimney. Oceanography 29(2):10–11, http://dx.doi.org/10.5670/oceanog.2016.27.

DOI http://dx.doi.org/10.5670/oceanog.2016.27

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First Evidence of Bioluminescence on a “Black Smoker” Hydrothermal Chimney

By Brennan T. Phillips, David F. Gruber, Ganesh Vasan, Vincent A. Pieribone, John S. Sparks, and Christopher N. Roman

ioluminescence in the deep sea in 2006 (Haymon et al., 2008). Outfitted moving quickly in one recording, indi- is omnipresent, yet imagery with the low-light camera and two high- cating a mobile organism. Review of of the phenomenon is scarce. power strobes oriented vertically toward footage obtained five minutes prior to the BWhile this dearth in observations can be the seafloor, the ROV was positioned low-light recordings revealed a relatively largely explained by sampling effort, the almost directly over the vent orifice of one low abundance of macrobiology on and camera technology available for in situ, of the larger active chimneys at 1,643 m around the chimney, with a few scattered low-light imagery is also a limiting fac- water depth (~1 m altitude, chimney Bythograeid crabs, squat lobsters, and tor. Recent work by Phillips et al. (2016) height 11 m). All lights on the ROV sys- numerous Alvinocarid shrimp. Based on describes the application of a Hamamatsu tem were turned off (including external these observations and the behavior of ORCA Flash2.0 V2 sCMOS camera to LED indicators), and closed-loop iner- the luminescence, it is likely biologically detect light-stimulated luminescence tial navigation control was used to main- sourced and could be a free-swimming in the water column. This system was tain vehicle position within <10 cm on all shrimp. Whether such an organism is a recently employed to observe biolumi- axes. The vehicle hovered over the chim- vent-associate or a member of the sur- nescence on a deep-sea “black smoker” ney for approximately 20 minutes while rounding midwater community cannot be hydrothermal vent. light-stimulation techniques, as per- determined by these observations alone. As part of a multidisciplinary expe- formed in Phillips et al. (2016), were used Blackbody radiation and visible light dition on E/V Nautilus aimed at explor- to elicit bioluminescent responses. No have been measured using various ing the Galápagos Spreading Center, dive light-stimulated bioluminescence was methods at several hydrothermal vents #H1439 on July 1, 2015, used the Hercules observed, but two recordings made as (Van Dover et al., 1996; White et al., remotely operated vehicle (ROV) system controls without any strobes detected a 2002). While the low-light camera used to take a close look at the Iguanas hydro- weak, mobile luminescent source within in this study can detect wavelengths up thermal vent field (Raineault et al., 2016). 1 m of the vent orifice (Figure 1, supple- into the near-infrared spectrum, no pat- This vent system was initially discovered mental video). The source appears to be terns were visible in our recordings. This may be attributed to the relatively low temperatures measured at the vent orifice (maximum reading 154.7°C) and the diminished quantum efficiency of the camera in the low infrared wavelength spectrum (800–1,000 nm). Given the absence of any solar radiation from the surface and negative observations of bioluminescence on vents by human observ- ers, it has been hypothesized that blackbody radiation from deep-sea vents may be a signal for vent shrimp to locate and/ or avoid heat sources through the use of primitive photoreceptor organs (Pelli and Chamberlain 1989; Van Dover et al., 1989; FIGURE 1. (left) Strobe-lit, down-looking view of the active black smoker chimney. (right) Same field of view as the strobe-lit image, with a single bioluminescent source visible in the lower-right corner. O’Neill et al., 1995; Nuckley et al., 1996). The location of the bioluminescent source is circled in red in both images. Given our observations of naturally

10 Oceanography | Vol.29, No.2 OceanographyUpcoming occurring bioluminescence directly adja- Phillips, B.T., D.F. Gruber, G. Vasan, C.N. Roman, V.A. Pieribone, and J.S. Sparks. 2016. Observations Special Issues cent to an active vent, it may be that such of in situ deep-sea marine bioluminescence photosensitive capabilities serve more with a high-speed, high-resolution sCMOS camera. Deep Sea Research Part I 111:102–109, than to simply locate and avoid extreme http://dx.doi.org/10.1016/j.dsr.2016.02.012. September 2016 heat sources. For example, Johnsen Raineault, N.A., R.D. Ballard, L. Mayer, C.R. Fisher, GoMRI Gulf Oil Spill & S. Carey, L. Marsh, R. Kane, S. Tüzün, T.M. Shank, Ecosystem Science et al. (1995) suggest that the measured and C. Smart. 2016. Exploration of hydrother- peak sensitivity of Rimicaris sp. shrimp mal vents along the Galápagos Spreading Center. Pp. 35–37 in New Frontiers in Ocean December 2016 at ~500 nm is more attuned to visible- Exploration: The E/V Nautilus and NOAA Ship Ocean-Ice Interaction spectrum light than blackbody radiation, Okeanos Explorer 2015 Field Season. K.L.C. Bell, M.L. Brennan, J. Flanders, N.A. Raineault, and which may be an artifact of their pro- K. Wagner, eds. Oceanography 29(1), supple- March 2017 posed evolution from surface-dwelling ment, http://dx.doi.org/10.5670/oceanog.2016. International Cooperation in supplement.01. Harmful Algal Bloom Science bresiliid shrimp (Chamberlain, 2000). Van Dover, C.L., E.Z. Szuts, S.C. Chamberlain, It is our hope that these crude obser- and J.R. Cann. 1989. A novel eye in ‘eyeless’ shrimp from hydrothermal vents of the Mid- June 2017 vations will stimulate further interest Atlantic Ridge. Nature 337(6206):458–460, TBN regarding the role of bioluminescence http://dx.doi.org/10.1038/337458a0. Van Dover, C.L., G.T. Reynolds, A.D. Chave, September 2017 within and around hydrothermal vent and J.A. Tyson. 1996. Light at deep- Sedimentary Processes Building a systems, with a possible focus on vent sea hydrothermal vents. Geophysical Research Letters 23(16):2,049–2,052, Tropical Delta Yesterday, Today, and shrimp as potential light-producing ani- http://dx.doi.org/10.1029/96GL02151. Tomorrow: The Mekong System mals. The continual improvement of White, S.N., A.D. Chave, G.T. Reynolds, and C.L. Van Dover. 2002. Ambient light emission December 2017 low-light scientific cameras used for in from hydrothermal vents on the Mid-Atlantic Celebrating 30 Years of Ocean Science situ imagery, paired with reliable and Ridge. Geophysical Research Letters 29(15), http://dx.doi.org/10.1029/2002GL014977. and Technology at the Monterey Bay precise vehicle navigation, makes such Aquarium Research Institute endeavors possible. ACKNOWLEDGMENTS This research used data provided by the Nautilus SUPPLEMENTAL MATERIAL Exploration Program, Expedition #NA064. The authors wish to thank the E/V Nautilus crew and A link to the video of the hydrothermal chimney col- the ROV team for their expertise and technical sup- lected by camera on ROV Hercules can be obtained port, the Inner Space Center at the University at http://dx.doi.org/10.5670/oceanog.2016.27. of Rhode Island, and Chuck Fisher for facilitat- ing this research. This work was conducted under REFERENCES research permit #PC-45-15, and the authors thank Chamberlain, S.C. 2000. Vision in hydrothermal the Galápagos National Park directorate and the vent shrimp. Philosophical Transactions of the Charles Darwin Research Station for their collabora- Royal Society of London B 355(1401):1,151–1,154, tion. Sheri White, Cindy Van Dover, and one anony- http://dx.doi.org/10.1098/rstb.2000.0657. mous reviewer contributed constructive comments Haymon, R.M., S.M. White, E.T. Baker, P.G. Anderson, that greatly enhanced this article. This work was K.C. Macdonald, and J.A. Resing. 2008. High- funded in part by the Ray and Barbara Dalio Family resolution surveys along the hot spot-affected Foundation and NSF grant DEB-1257555 to JSS. Gálapagos Spreading Center: 3. Black smoker dis- coveries and the implications for geological controls on hydrothermal activity. Geochemistry, AUTHORS Brennan T. Phillips ([email protected]) Geophysics, Geosystems 9, Q12006, is PhD Candidate, University of Rhode Island, http://dx.doi.org/10.1029/2008GC002114. Graduate School of Oceanography, Narragansett, In addition to the special issues articles, Johnson, M.L., P.M.J. Shelton, P.J. Herring, RI, USA. David F. Gruber is Associate Professor, City and S. Gardner. 1995. Spectral responses Oceanography solicits and publishes: University of New York, Baruch College, New York, from the dorsal organ of a juvenile Rimicaris • Peer-reviewed articles that chronicle NY, USA. Ganesh Vasan is Postdoctoral Associate, exoculata from the TAG hydrothermal vent site. The John B. Pierce Laboratory, New Haven, CT, USA. all aspects of ocean science and its BRIDGE Newsletter 8:38–42. Vincent A. Pieribone is Fellow, The John B. Pierce applications Nuckley, D.J., R.N. Jinks, B.A. Battelle, E.D. Herzog, Laboratory, New Haven, CT, USA, and Professor, L. Kass, G.H. Renninger, and S.C. Chamberlain. • News and information, meeting reports, Cellular and Molecular Physiology & Neurobiology, 1996. Retinal anatomy of a new species of bresiliid hands-on laboratory exercises, career Yale University School of Medicine, New Haven, shrimp from a hydrothermal vent field on the Mid- profiles, and book reviews CT, USA. John S. Sparks is Curator-in-Charge, Atlantic Ridge. The Biological Bulletin 190(1):98–110. American Museum of Natural History, New York, NY, • Editor-reviewed articles that address O’Neill, P.J., R.N. Jinks, E.D. Herzog, B.A. Battelle, USA. Christopher N. Roman is Assistant Professor, L. Kass, G.H. Renninger, and S.C. Chamberlain. public policy and education and how University of Rhode Island, Graduate School of 1995. The morphology of the dorsal eye they are affected by science and Oceanography, Narragansett, RI, USA. of the hydrothermal vent shrimp, Rimicaris technology exoculata. Visual Neuroscience 12(05):861–875, • Breaking Waves articles that describe http://dx.doi.org/10.1017/S0952523800009421. ARTICLE CITATION novel approaches to multidisciplinary Pelli, D.G., and S.C. Chamberlain. 1989. The vis- Phillips, B.T., D.F. Gruber, G. Vasan, V.A. Pieribone, ibility of 350°C black-body radiation by J.S. Sparks, and C.N. Roman. 2016. First evidence problems in ocean science the shrimp Rimicaris exoculata and man. of bioluminescence on a “black smoker” hydro- Nature 337(6206):460–461, http://dx.doi.org/ thermal chimney. Oceanography 29(2):10–11, 10.1038/337460a0. http://dx.doi.org/10.5670/oceanog.2016.27. http://www.tos.org/ Oceanography | June 2016 11 oceanography